Public good dynamics drive evolution of iron acquisition strategies in natural bacterioplankton populations

Abstract

A common strategy among microbes living in iron-limited environments is the secretion of siderophores, which can bind poorly soluble iron and make it available to cells via active transport mechanisms. Such siderophore-iron complexes can be thought of as public goods that can be exploited by local communities and drive diversification, for example by the evolution of "cheating." However, it is unclear whether bacterial populations in the environment form stable enough communities such that social interactions significantly impact evolutionary dynamics. Here we show that public good games drive the evolution of iron acquisition strategies in wild populations of marine bacteria. We found that within nonclonal but ecologically cohesive genotypic clusters of closely related Vibrionaceae, only an intermediate percentage of genotypes are able to produce siderophores. Nonproducers within these clusters exhibited selective loss of siderophore biosynthetic pathways, whereas siderophore transport mechanisms were retained, suggesting that these nonproducers can act as cheaters that benefit from siderophore producers in their local environment. In support of this hypothesis, these nonproducers in ironlimited media suffer a significant decrease in growth, which can be alleviated by siderophores, presumably owing to the retention of transport mechanisms. Moreover, using ecological data of resource partitioning, we found that cheating coevolves with the ecological specialization toward association with larger particles in the water column, suggesting that these can harbor stable enough communities for dependencies among organisms to evolve. microbial diversity | ocean bacteria | population structure |

Microbial Speciation

“…Although such relationships have been shown for several, divergent groups of bacteria, in some archaea, the requirement for short, identical DNA stretches seems to be absent (Grogan and Stengel 2008;Naor et al 2012), even though environmental observations support decreased rates of recombination across clusters (Whitaker et al 2005;Williams et al 2012). Moreover, recent comparison of very closely related genomes has also shown that very little sequence similarity appears to be required for integration of long stretches of highly divergent DNA (including single nucleotide changes and structural variants) into the genome (Mell et al 2011;Cordero et al 2012a), although the mechanisms remain unclear. These recent results show that much remains to be learned about how recombination proceeds in different groups of bacteria and archaea, making mathematical models an important tool to explore potential outcomes, given reasonable assumptions about the importance of recombination relative to mutation and selection.…”

“…4 (In fact, the distinction might not be so clear. There is mounting evidence that homologous recombination is often involved in gene addition and loss [de Vries and Wackernagel 2002;Mell et al 2011;Cordero et al 2012a;Croucher et al 2012].) Importantly, the rates and bounds of this gene transfer can vary considerably.…”

Long-term social dynamics drive loss of function in pathogenic bacteria

“…Furthermore, an intriguing experimental demonstration of the potential clinical relevance of microbial social interactions comes from the work by Koch et al (29), which showed that intraspecific competition can select for antibiotic-resistant Staphylococcus aureus bacteria in the absence of antibiotic pressure. Together with studies on cooperator-cheat dynamics in natural populations of bacteria, such as iron acquisition of Vibrio in seawater (30) and toxin production in Bacillus infecting moth larvae (31), this finding calls for a reevaluation of how we interpret evolutionary change of natural microbial populations.…”

Antibiotic stress selects against cooperation in the pathogenic bacterium Pseudomonas aeruginosa

“…evolution | cooperation | antibiotics | social behavior | resistance P ublic goods production is a characteristic of a diverse range of taxa, from microbes to humans (1)(2)(3). Explaining the persistence of this costly behavior is challenging, because cheats can exploit the commons without contributing.…”